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Testosterone Secretion, Musth Behaviour and Social Dominance in Captive Male Asian Elephants Living Near the Equator G

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Testosterone Secretion, Musth Behaviour and Social Dominance in Captive Male Asian Elephants Living Near the Equator G Testosterone secretion, musth behaviour and social dominance in captive male Asian elephants living near the equator G. A. Lincoln and W. D. Ratnasooriya 1MRC Reproductive Biology Unit, Centre for Reproductive Biology, 37 Chalmers Street, Edinburgh EH3 9EW, UK; and 2Department of Zoology University of Colombo, PO Box 1490, Colombo 3, Sri Lanka Testosterone concentrations were measured in blood samples collected weekly over a 5 year period from six adult (19\p=n-\40year old) male Asian elephants (Elephas maximus maximus) living in captivity in Sri Lanka (7\s=deg\N),to investigate the relationship between androgen secretion and the occurrence of musth (temporal gland secretion, drip urination and aggressive behaviour). The testosterone profiles were very variable both within and between animals. Long-term phasic changes in blood concentrations of testosterone, associated with periods of musth, occurred in three of the six elephants, with the most pronounced cyclicity in the oldest animal. Musth occurred annually after periods of high androgen secretion and there was a positive correlation between the duration of musth and mean concentrations of testosterone during the previous 2 months. The time of musth, while consistent for an individual, was variable between animals. In four bulls living within one social group, there was a positive correlation between social rank and mean concentrations of testosterone over the 5 year study, and only the dominant animal showed periodic musth. Short-term changes in testosterone concentrations occurred in blood samples collected every 15 min for 7 h, and following the injection of 20 \g=m\gGnRH, consistent with regulation through the pulsatile secretion of LH. Overall, the results support the view that fully mature male Asian elephants living near the equator express an asynchronous, cyclical, circannual pattern of gonadal activity, with the cyclical pattern developing progressively from 20 to 40 years of age. The periodic increase in testosterone secretion during the gonadal cycle induces the development of musth; however, androgen withdrawal following a period of hypersecretion may be the cause of some aspects of musth behaviour (aggression, unpredictability, disobedience) which make bull elephants very difficult to manage in captivity. Introduction year; however, there is no synchrony between individuals in the population, and there may be males in musth at all times of The phenomenon of musth is best documented in captive male the year (Poole, 1994). In captivity, male Asian elephants in Asian elephants (Elephas maximus) but also occurs in male musth can be very dangerous and unmanageable, and are restrained with chains from with African elephants (Loxodonta africana), and is a natural feature of usually kept away contact the life cycle in the wild for both species (McCaughey, 1963; people (Eisenberg et al, 1971). Poole and Moss, 1981; Poole, 1994). Musth appears to be There have been only a few longitudinal studies that similar to rutting behaviour in ungulates (Poole, 1987) and is document the long-term changes in testosterone secretion associated with periodic increases in testosterone secretion associated with musth in male elephants. For practical reasons, (Jainudeen et al, 1972a; Hall-Martin and van der Walt, 1984; these have involved animals living in captivity at latitudes well Cooper et al, 1990; Niemuller and Liptrap, 1991). During outside the normal range for the species (for example, Asian musth, males spend less time feeding, leave the bachelor herd, and African elephants in Columbus Zoo, Powel, Ohio, USA at wander long distances in search of females in oestrus, become 50°N, Cooper et al, 1990; Asian elephants in captivity in aggressive towards other males, vocalise with infrasound, Ontario, Canada at 54°N; Niemuller and Liptrap, 1991). Thus, produce copious secretions from the enlarged temporal glands the purpose of the current study was to assess the pattern of and drip urine from the prepuce. Most matings are achieved cyclicity under equatorial conditions by documenting the during this phase (Hall-Martin, 1987; Poole, 1989). The older changes in blood concentrations of testosterone and behaviour bulls usually come into musth annually at a specific time of over 5 years in male Asian elephants living in captivity in Sri Lanka. This was a collaborative study between the National Received 8 March 1996. Zoological Gardens based in Colombo, the Department of Downloaded from Bioscientifica.com at 10/02/2021 04:07:02AM via free access Zoology, University of Colombo, Sri Lanka, and the Univer¬ sities Federation for Animal Welfare (UFAW) based in London, with the overall objective of developing more humane ways of managing male elephants in musth and of improving the success of breeding Asian elephants in captivity (Poole et al, in press). Materials and Methods Animals and sampling Six adult, male Asian elephants of the Sri Lankan subspecies (Elephas maximus maximus) were used in the study which was conducted from 1986 to 1991. The animals were cared for individually by mahouts and lived in two different social envi¬ ronments (see Fig. 1). Two males, EHM (Bandula, 40 years in 1986) and E12 (Sampath, 20 years) were housed within the National Zoological Gardens in Colombo, Sri Lanka (6°54'N, 79°52'E). They were normally kept tethered in an open building alongside females, but were paraded for the public and bathed twice a day. Food, consisting of trunks and branches of Caryota arena, leaves and woody parts of Artocarpus heterophyllus and Cocos nucífera, was provided in the evening. The other four elephants, E3M (Wijaya, 22 years), E4M (Kadira, 19 years), E5M (Jandura, 19 years) and E6M (Neela, 20 years) lived in the Pinnawala Elephant Orphanage about 50 miles north of Colombo. The animals were also tethered overnight, but during the day they were released into a 12 hectare coconut plantation to feed along with a group of six adult female and at least twenty young elephants (Fig. 1). Supplementary food consisted of approximately 76 kg foliage at night and 2 kg food mixture (maize meal, rice bran, powdered ginger seed and minerals) in the middle of the day. All the animals at the Orphanage were walked approximately 1 km in the morning and evening to bath in a shallow river. The ages of the five younger animals were known accurately as they were taken from the wild as juveniles, or born in captivity. The age of the older elephant was esti¬ mated by the experienced mahout based on body size and tooth eruption. All animals were of adult body size (Fig. 1) but the exact height and weight were not determined. Blood samples were collected at 09.00—10.00 h at weekly intervals by the staff of the National Zoological Gardens. The procedure involved the mahout instructing the elephant to lie down to permit a blood sample (5-10 ml) to be withdrawn from a vein on the back of the ear. The animals were habituated to the sampling and were normally compliant even during periods of musth, thus no special techniques were used to restrain the animals which might have influenced the patterns of hormone secretion. The blood was allowed to clot for 1—2 h Fig. 1. (a) E12M (Sampath, 24 years old) in National Zoological at room temperature (28—31°C) before centrifugation at Gardens, Colombo, Sri Lanka showing musth in July 1990 associ¬ ated with blood concentrations of see 2. 3 000 rpm for 15 min, and the serum was stored at 20°C. On high testosterone, Fig. — He was chained to a tree because of his increased one occasion, blood were collected at 15 min intervals aggressiveness, samples (b) Dominant E3M 26 old, in the for 9 h from two of the (E4M and E6M) to monitor elephant (Wijaya, years right) elephants Pinnawala Elephant Sri Lanka social interaction short-term fluctuations in testosterone secretion, and at 15 min Orphanage, showing with the next most dominant bull E6M (Neela, 24 years, left) in intervals for 2 h from all six to monitor the elephants response May 1991. (c) E4M (Kadira, 23 years old) showing the daytime a standardised to injection of GnRH (20 µg GnRH per elephant behaviour in the coconut plantation in Pinnawala Elephant i.v., Cambridge Research Biochemical, Northwich). For this, the Orphanage with close proximity between elephants. Note the elephants were walked alongside a raised platform, and blood absence of large tusks, a feature of most fully mature bull elephants samples were collected by venepuncture from a vein on the in Sri Lanka. Downloaded from Bioscientifica.com at 10/02/2021 04:07:02AM via free access back of the ear with the animal in a standing position. The samples were heparinised, centrifuged at 3000 rpm for 15 min within 60 min, and the plasma samples were stored at 20°C. — All serum and plasma samples were transported frozen from Sri Lanka to Edinburgh, UK for the measurement of testosterone concentrations by radioimmunoassay. The behavioural characteristics of the elephants were assessed by the curator and mahouts, and recorded weekly. Individuals were classified as in musth when they showed at least two of the following features: enlarged temporal glands with continuous secretion; dripping urine; loss of appetite and restless behaviour; unusually aggressive behaviour to people or other animals. Detailed, twice monthly recordings of the interactions between adult elephants in the Pinnawala Orphanage were also made for 21 months from October 1986 (Poole et al, in press). Radioimmunoassays The concentrations of testosterone in the serum and plasma samples collected from the elephants were measured in dupli¬ cate by radioimmunoassay using the method of Corker and Davidson (1978), as modified by Sharp and Bartlett (1985) for iodinated tracer. The limit of detection of the assay was 0.1 ng ml- and the intra- and interassay coefficients of variation (CV) were 6.8% and 10.0%, respectively.
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